Obstetrics & Gynecology:
Predictors of Cesarean Delivery for Periviable Neonates
Tucker Edmonds, Brownsyne MD, MPH; Fager, Corinne MS; Srinivas, Sindhu MD, MSCE; Lorch, Scott MD, MSCE
From the University of Pennsylvania, Robert Wood Johnson Foundation Clinical Scholars Program, Department of Obstetrics and Gynecology, Philadelphia, Pennsylvania; Children's Hospital of Philadelphia, Philadelphia, Pennsylvania; the University of Pennsylvania, Maternal and Child Health Research Program, Department of Obstetrics and Gynecology, Center for Research on Reproduction and Women's Health, Leonard Davis Institute, Philadelphia, Pennsylvania; and the University of Pennsylvania School of Medicine, Department of Pediatrics, Division of Neonatology, Children's Hospital of Philadelphia, Center for Outcomes Research, Leonard Davis Institute, Philadelphia, Pennsylvania.
Dr. Tucker Edmonds' salary is supported by the Robert Wood Johnson Foundation Clinical Scholars Program. The study is supported by the following granting agencies: MCHB R40 MC 05474 and AHRQ R01 HS 05696.
Corresponding author: Brownsyne Tucker Edmonds, University of Pennsylvania, 1303 Blockley Hall, 423 Guardian Drive, Philadelphia, PA 19104; e-mail: firstname.lastname@example.org.
Financial Disclosure The authors did not report any potential conflicts of interest.
OBJECTIVE: To test for racial or ethnic disparities or both in periviable cesarean delivery and describe sociodemographic and clinical characteristics associated with periviable cesarean delivery.
METHODS: This was a retrospective cohort study of state-level maternal and neonatal hospital discharge data linked to vital statistics data for deliveries occurring between 23.0 and 24.6 weeks of gestation in California, Missouri, and Pennsylvania from 1995 to 2005 (N=8,290).
RESULTS: Approximately 79% of the population was aged 18–35 years, and almost half were nulliparous. Almost 20% of the women were African American, 36.4% were Hispanic, and 33.6% were white. Overall, 33.6% of periviable neonates were delivered by cesarean. In multivariable analyses adjusting for sociodemographic and clinical characteristics, cesarean delivery did not differ among African American and Hispanic women compared with white women (odds ratio [OR] 0.89, 95% confidence interval [CI] 0.76–1.05; and OR 0.95, 95% CI 0.83–1.09, respectively). Women presenting with preterm labor were significantly less likely to undergo cesarean delivery (OR 0.84, 95% CI 0.73–0.96), whereas women presenting with preterm premature rupture of membranes (OR 1.29, 95% CI 1.14–1.45) or abruption (OR 2.43, 95% CI 2.09–2.81) were more likely to have cesarean deliveries. The strongest predictor of periviable cesarean delivery was pregnancy-induced hypertension (OR 15.6.4, 95% CI 12.3–19.7).
CONCLUSION: Unlike disparities observed at later gestational ages, cesarean delivery did not differ by race and ethnicity among this periviable cohort. Instead, medical indications such as pregnancy-induced hypertension, preterm premature rupture of membranes, or abruption were associated with a higher likelihood of cesarean delivery. Periviable deliveries represent a subset of deliveries, wherein race and ethnicity do not influence mode of delivery; the acuity of the clinical encounter dictates the course of care.
LEVEL OF EVIDENCE: II
A growing number of studies demonstrate racial or ethnic disparities or both in mode of delivery.1–9 Among both term and preterm cohorts, non-Hispanic African American women have experienced greater increases in cesarean delivery rates than their non-Hispanic white counterparts.9 However, such trends have been examined only among deliveries occurring at or beyond 28 weeks of gestation. Racial or ethnic disparities in cesarean delivery trends have not been examined among extremely preterm deliveries.
A subset of extremely preterm deliveries that warrants increased attention is the group performed at the threshold of viability. Periviable neonates achieve poor survival rates and suffer poor neurologic outcomes, resulting in substantial emotional and financial costs to families and the health care system.10–12 Although a recent study suggests a slight survival advantage for periviable neonates delivered by cesarean,13 performing cesarean delivery for periviable fetuses remains controversial in light of the potential maternal morbidity associated with classical cesarean delivery and its long-term implications for future deliveries.14,15
With such uncertainty surrounding the management and outcomes of periviable deliveries, it remains unclear what factors contribute to decisions about mode of delivery for periviable fetuses. We performed a retrospective cohort analysis to test for racial and ethnic differences in utilization of cesarean delivery for periviable fetuses. We hypothesize that African American and Hispanic women are more likely to undergo cesarean delivery. As a secondary aim, we examine additional sociodemographic, clinical, and diagnostic categories to describe predictors of periviable cesarean delivery.
MATERIALS AND METHODS
We conducted a retrospective cohort study, analyzing state-level maternal and neonatal hospital discharge data linked to birth and death certificate data, for California, Missouri, and Pennsylvania from 1995 to 2005. The institutional review boards of the departments of health in California, Missouri, and Pennsylvania and the Children's Hospital of Pennsylvania approved this study. The records were created by linking birth certificate data with maternal hospital discharge records and newborn hospital discharge records or death certificate data in the event of a fetal demise. Records were linked using a previously described method, wherein a mixture of deterministic and probabilistic approaches were used to match records with a virtual identifier based on variables common to both datasets.16 This technique has been shown to be valid and reproducible, and, in subsequent studies, more than 98% of birth and death certificates were matched to maternal and newborn hospital records when the technique was applied.17
Live singleton births and “in-hospital” fetal deaths occurring between 23.0 and 24.6 weeks of reported gestational age were included in the analysis. Gestational age variables were missing in approximately 8% of the data. To use all available data, we also included neontates with birth weights that reasonably could have occurred at a gestational age between 23 and 24.6 weeks assessed using available fetal growth curves.18 To estimate the missing gestational ages, we used a linear regression model containing birth weight, sociodemographic characteristics, neonatal characteristics, maternal comorbidities, and maternal complications. In cases in which a decision is reached not to resuscitate a fetus, a periviable pregnancy more likely would result in a vaginal delivery and a fetal, rather than a neonatal, death. As a result, not examining in-hospital fetal deaths could result in biased results if there are racial or ethnic differences or both in the choice to resuscitate a periviable fetus, as a previous study suggests.19 Therefore, it was important that fetal deaths not be excluded entirely from the analysis. We sought to distinguish these types of fetal deaths from fetal deaths that occurred out of hospital or as intrauterine demises. Deaths were designated as “outpatient” or “intrauterine” fetal deaths using criteria described by Phibbs et al in previous work20 and excluded from the analysis (Appendix 1).
The outcome of interest for this study was cesarean delivery (International Classification of Diseases, 9th Revision, Clinical Modification [ICD-9-CM] codes 669.7x and 74.x), which had to be documented in the maternal or neonatal record. Ultimately, documentation of 99% of cesarean deliveries was obtained from the maternal record. The primary predictor of interest was maternal race or ethnicity, designated in four categories: white, African American, Hispanic, and other. Maternal sociodemographic characteristics, including age in three categories (younger than 18 years, 18–35 years, older than 35 years); parity in four categories (0, 1, 2, 3 or more), education in two categories (less than a high school education or at least a high school education), median annual zip code income (determined based on zip code: Less than or equal to $20,000, greater than $20,000 to less than or equal to $40,000 ($20,000.01–$40,000.00), greater than 40k to less than equal to $60,000 ($40,000.01–$60,000.00), greater than $60,000) to approximate household income, early prenatal care (defined as entry at 0–3 months), and insurance payer (fee for service, health maintenance organization, federally insured, uninsured, and other) were included as covariates. Maternal comorbidities, pregnancy complications, and delivery indications included in the full model were pre-existing diabetes mellitus, gestational diabetes mellitus, chronic hypertension, pregnancy-induced hypertension (PIH), preterm labor, preterm premature rupture of membranes (PROM), placental abruption, repeat cesarean, placenta previa, and malpresentation. The ICD-9-CM codes used for specific diagnoses are listed in Appendix 2. Fetal anomalies are excluded because anomaly diagnoses are only documented in the records for live births. There were no racial differences with any fetal anomalies.
All analyses were performed using SAS 9.2. χ2 tests were used to assess univariable associations with outcome. Logistic regression was performed for multivariable analyses. Logistic regression models were built in sequence, first controlling for sociodemographic factors that might confound the relationship between race or ethnicity or both and cesarean delivery; then additionally controlling for potential confounding by adding maternal comorbid conditions; and finally, adding pregnancy complications and delivery indications. Covariates were included in the model based on a priori assumptions about clinical relevance and face validity, which were supported by our review of the literature and collective clinical experience.1,21–24 We included delivery hospital as a fixed effect in the model to account for the potential effect of clustering at the level of the delivery hospital. Hospital identifications were included in the model if at least 25 deliveries occurred in the hospital. Hospitals with fewer than 25 deliveries were grouped by state and represented in the model as three “small hospital” variables because of wide variation in the outcomes at small hospitals.25 Last, as an additional sensitivity analysis, we conducted the analyses, stratifying by states, to ensure that grouping the states did not dilute the effect estimates.
For the ease of interpretation, odds ratios (ORs) calculated from logistic regression analyses were transformed into standardized proportions using marginal standardization.26 These standardized proportions are interpreted as the estimated probability of cesarean delivery if the entire cohort were alternatively subjected to the risk factor or not subjected to the risk factor. For each risk factor, the number needed to treat was calculated by taking the reciprocal of the risk difference, which is the difference between the expected probabilities for risk factor and nonrisk factor groups. We present these estimates in addition to ORs for our results.
Our study population comprised 8,290 maternal–neonatal observations. California contributed 76.4% (6,332) of the deliveries; Missouri contributed 8.4% (694); and Pennsylvania contributed 15.3% (1,264). Tables 1 and 2 provide baseline sociodemographic and clinical characteristics for the mother and newborn pairs that compose the study cohort. Approximately 79% of the maternal population was age 18–35 years, and almost half were nulliparous. Almost 20% of the women were African American, 36.4% were Hispanic, and 33.6% were white. Roughly 30% had less than a high school education, and almost half were federally insured. Overall, 33.6% of women underwent cesarean delivery.
Women who were delivered by cesarean differed significantly from those who were not delivered by cesarean across sociodemographic categories such as age and parity. A total of 39.0% of women older than 35 years were delivered by cesarean compared with 33.2% of 18- to 35-year-olds and 28.1% of teenagers (P<.001). Likewise, there was a trend toward higher percentages of cesarean deliveries among women with higher parity (P<.001). Mode of delivery also differed based on maternal comorbidities. Compared with women who delivered vaginally, women delivered by cesarean were more likely to have PIH (15.7% compared with 2.12%, P<.001), chronic hypertension (2.19% compared with 1.09%, P<.001), and gestational diabetes mellitus (2.52% compared with 1.74%, P=.02). Notably, the percentage of women undergoing cesarean delivery did not differ significantly across racial or ethnic groups (P=.839).
Table 3 displays the results of multivariable logistic regression models adjusting for maternal sociodemographic characteristics. In these models, women of African American, Hispanic, and other racial or ethnic groups were somewhat less likely to undergo cesarean delivery, but the odds were not statistically different from those of white women (OR for African American women 0.89, 95% confidence interval [CI] 0.76–1.05; OR for Hispanic women 0.95, 95% CI 0.83–1.09; OR for other racial or ethnic groups 0.87, 95% CI 0.72–1.06 in full model). These ORs translate to roughly one in three women undergoing cesarean deliveries among each racial or ethnic group (expected probabilities 0.33 for African American, 0.34 for Hispanic, 0.32 for other racial or ethnic group, and 0.34 for white). In the full models, high parity (three or more) is the only sociodemographic characteristic consistently associated with having lower odds of cesarean delivery (Table 4).
Ultimately, maternal comorbidities and pregnancy complications were found to be the strongest predictors of cesarean delivery. Women presenting with preterm labor were significantly less likely to undergo cesarean delivery (OR 0.84, 95% CI 0.73–0.96, risk difference 0.03), which translates to one fewer cesarean delivery for every 35 women presenting with preterm labor. Women presenting with preterm PROM or abruption were more likely to have cesarean deliveries (OR 1.29 95% CI 1.14–1.45, risk difference 0.04, and OR 2.43, 95% CI 2.09–2.81, risk difference 0.15, respectively). Therefore, one additional cesarean delivery was performed for every 25 women presenting with preterm PROM and every 6 women presenting with placental abruption. The strongest predictor of periviable cesarean delivery was PIH. Women with PIH had 15.6 times the odds of cesarean delivery than women without PIH (95% CI 12.3–19.7, risk difference 0.49), suggesting that an additional cesarean delivery was performed for every two women who presented with PIH. Indications for cesarean delivery, including previa, repeat cesarean delivery, and malpresentation placed women at 5 to 6 times the odds of undergoing cesarean delivery, which added a cesarean delivery for every three women presenting with these indications (risk differences 0.30 for previa, 0.33 for repeat cesarean, and 0.31 for malpresentation). Last, women presenting at a gestational age between 24 and 24.6 weeks had more than twice the odds of cesarean delivery compared with women presenting between 23 and 23.6 weeks of gestation (OR 2.14, 95% CI 1.92–2.39, risk difference 0.12), which translates to an additional cesarean delivery for every eight neonates born between 24 and 24.6 weeks. Neither adjusting for delivery hospital nor stratifying the analysis by state changed these findings.
We hypothesized that African American and Hispanic women at periviable gestational ages would be more likely to undergo cesarean delivery. However, neither race, nor any other sociodemographic characteristics, was associated with cesarean delivery. Instead, we found that clinical presentation was the strongest predictor of cesarean delivery.
These findings add to the body of literature that considers the role of race in cesarean decision-making. Previous studies demonstrate racial or ethnic disparities in mode of delivery.1–8 Braveman and colleagues' study of more than 200,000 primiparous women found that African American women were 24% more likely to undergo cesarean delivery than white women, even after controlling for sociodemographic characteristics, insurance status, medical indications, and hospital characteristics.3 Scott-Wright and colleagues examined a cohort of college-educated African American and white women and found that, even with comparable levels of education, African American women had 1.78 times the odds of cesarean delivery than their white counterparts.27 And more recently, Bryant et al studied the delivery experience of more than 28,000 women delivering in a tertiary care center and found that, controlling for known risks, African American women and Hispanic women had 1.48 and 1.19 times the odds of cesarean delivery, respectively.28 These disparities have been found primarily among term deliveries. Our findings suggest that periviable deliveries represent a subset of deliveries wherein race or ethnicity does not predict mode of delivery, but rather, the acuity of the clinical encounter dictates the course of care. For example, preeclampsia, which was the strongest predictor of cesarean delivery, demands prompt delivery for maternal, rather than fetal, benefit when women present with severe forms.
Patient preference has been considered as a potential explanation for racial differences observed in term cesarean delivery rates. Previous work found that among nonpregnant women surveyed about preferences for route of delivery, 21.7% of nonwhite women compared with 7.8% of white women preferred cesarean delivery (P=.03).29 We formulated our hypothesis, in part, on the basis of the premise that patient preference plays a central role in determining mode of delivery when managing periviable deliveries. We assumed that just as African American and Hispanic adults prefer heroic measures and interventional therapies in end-of-life decision-making, they would also prefer to have “everything done” in managing periviable delivery and resuscitative care.30–37 However, our study found that African American and Hispanic women delivering between 23 and 25 weeks of gestation had slightly lower odds of delivering by cesarean delivery compared with white women. This difference was not statistically different from white women. These findings suggest that the option for cesarean delivery may be less subject to patient preference in the periviable window. Patients frequently present with complications that warrant operative intervention independent of parental resuscitation preferences. Although obstetricians report that patient preference should play a role in resuscitation decisions,38 operative decision-making in this context appears to depend most heavily on the clinical presentation. Patient preference is also constrained by the options presented to patients. Obstetricians may not even offer the option of cesarean delivery below a threshold gestational age or under certain clinical scenarios.
As a retrospective cohort study, there are several limitations to the conclusions we can draw from these findings. Owing to the limitations of the data and the variables available in the data set, we are ultimately unable to determine whether the patterns of cesarean delivery observed reflect institutional practice, maternal preference, or physician guidance. We control for hospital effects with a fixed-effects model that revealed no differences in the findings. This suggests that institutional practice may be less of a driving factor. However, we cannot exclude the possibility that paternalism, bias, or perceived patient preference (rather than stated patient preference) on the part of physicians may lead some physicians to be less inclined to provide aggressive care, such as cesarean delivery, for socially disadvantaged women given the expense associated with neonatal intensive care and, potentially, caring for a disabled child. This could serve as an alternative explanation for the reversal in cesarean delivery trends seen in this periviable cohort compared with previous studies. Another limitation of the study is that we identified our predictor and outcome variables by ICD-9-CM codes, not primary chart abstraction. This creates the risk for misclassification. However, this method allows for a large, population-based cohort that is needed to study racial differences in this relatively rare event. Finally, other unmeasured confounders may play a significant role in decision-making and actually account for associations that we observed. However, this is less of a concern with a statistically nonsignificant result.
In conclusion, utilization of cesarean delivery did not differ by race or ethnicity in this cohort of periviable deliveries. Although the utility of performing cesarean deliveries for fetal benefit at periviable gestational ages remains in question, our findings highlight that cesarean delivery is frequently performed when clinical acuity or maternal benefit warrants prompt intervention. The findings of this study point to the complexity of clinical decision-making and to the need for greater understanding of how social and clinical factors are weighed and prioritized in cesarean decision-making.
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“Outpatient” or “intrauterine” fetal deaths were designated by the following International Classification of Diseases, 9th Revision, Clinical Modification codes using criteria described by Phibbs et al in previous work.15 Fetal deaths with these diagnoses were excluded from the analysis:
Papyraceous fetus: 646.01
Intrauterine death: 656.40, -41, or -43
Decreased fetal movement: 655.71
Cord entanglement with compression: 663.20
Cord entanglement without compression: 663.31
Ruptured uterus before delivery: 665.01
Insertion of laminaria: 69.93
Hysterotomy to terminate pregnancy: 74.91
The following International Classification of Diseases, 9th Revision, Clinical Modification codes were used to designate maternal and fetal characteristics included as covariates in the models:
Preexisting diabetes mellitus: 250.xx, 648.0x, 357.2, 362.0, 362.01, 362.02, 366.41
Gestational diabetes: 648.8x
Chronic hypertension: 642.0x, 642.1x, 642.2x
Pregnancy-induced hypertension: 642.4x, 642.5x, 642.7x
Preterm labor: 644.0x, 644.2x
Preterm premature rupture of membranes: 658.1x, 658.2x
Placental abruption: 641.2x
Repeat cesarean: 654.2x and birth certificate indicator
Placenta previa: 641.0x, 641.1x
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